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A tryptophan amphiphilic tetramerization domain-containing acetylcholinesterase from the bovine lungworm, Dictyocaulus viviparus

Published online by Cambridge University Press:  24 May 2006

J. B. MATTHEWS ,
O. LAZARI ,
A. J. DAVIDSON ,
S. WARREN  and
M. E. SELKIRK
J. B. MATTHEWS
Affiliation:
Division of Parasitology, Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 0PZ
O. LAZARI
Affiliation:
Veterinary Medicine Biology, Pfizer Animal Health, Sandwich, Kent CT13 9NJ
A. J. DAVIDSON
Affiliation:
Division of Parasitology, Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 0PZ
S. WARREN
Affiliation:
Division of Parasitology, Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 0PZ
M. E. SELKIRK
Affiliation:
Division of Cell and Molecular Biology, Imperial College London, London SW7 2AZ
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Abstract

Acetylcholine (ACh) is one of an array of neurotransmitters used by invertebrates and, analogous to vertebrate nervous systems, acetylcholinesterase (AChE) regulates synaptic levels of this transmitter. Similar to other invertebrates, nematodes possess several AChE genes. This is in contrast to vertebrates, which have a single AChE gene, transcripts of which are alternatively spliced to produce different types of the enzyme which vary at their C-termini. Parasitic nematodes have a repertoire of AChE genes which include those encoding neuromuscular AChEs and those genes which code for secreted AChEs. The latter proteins exist as soluble monomers released by the parasite during infection and these AChE are distinct from those enzymes which the nematodes use for synaptic transmission in their neuromuscular system. Thus far, Dictyocaulus viviparus is the only animal-parasitic nematode for which distinct genes that encode both neuromuscular and secreted AChEs have been defined. Here, we describe the isolation and characterization of a cDNA encoding a putative neuromuscular AChE from D. viviparus which contains a tryptophan amphiphilic tetramerization (WAT) domain at its C-terminus analogous to the common ‘tailed’ AChE form found in the neuromuscular systems of vertebrates and in the ACE-1 AChE from Caenorhabditis elegans. This enzyme differs from the previously isolated, D. viviparus neuromuscular AChE (Dv-ACE-2), which is a glycosylphosphatidylinositol-anchored variant analogous to vertebrate ‘hydrophobic’ AChE.

Keywords

Dictyocaulus viviparusnematodeacetylcholinesterasetryptophan amphiphilic tetramerization domain
Type
Research Article
Information
Parasitology , Volume 133 , Issue 3 , September 2006 , pp. 381 - 387
Copyright
2006 Cambridge University Press

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References

REFERENCES

Arpagaus, M., Fedon, Y., Cousin, X., Chatonnet, A., Berge, J. B., Fournier, D. and Toutant, J. P. ( 1994). cDNA sequence, gene structure, and in vitro expression of ace-1, the gene encoding acetylcholinesterase of class A in the nematode Caenorhabditis elegans. The Journal of Biological Chemistry 269, 9957–9965.Google Scholar
Belbeoc'h, S., Falasca, C., Leroy, J., Ayon, A., Massoulie, J. and Bon, S. ( 2004). Elements of the C-terminal t peptide of acetylcholinesterase that determine amphiphilicity, homomeric and heteromeric associations, secretion and degradation. European Journal of Biochemistry 271, 1476–1487.CrossRefGoogle Scholar
Bon, S., Dufourcq, J., Leroy, J., Cornut, I. and Massoulie, J. ( 2004). The C-terminal t peptide of acetylcholinesterase forms an alpha helix that supports homomeric and heteromeric interactions. European Journal of Biochemistry 271, 33–47.CrossRefGoogle Scholar
Chang, S. and Opperman, C. H. ( 1991). Characterization of acetylcholinesterase molecular forms of the root-knot nematode, Meloidogyne. Molecular and Biochemical Parasitology 49, 205–214.CrossRefGoogle Scholar
Combes, D., Fedon, Y., Grauso, M., Toutant, J. P. and Arpagaus, M. ( 2000). Four genes encode acetylcholinesterases in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae: cDNA sequences, genomic structures, mutations and in vivo expression. Journal of Molecular Biology 300, 727–742.CrossRefGoogle Scholar
Combes, D., Fedon, Y., Toutant, J. P. and Arpagaus, M. ( 2003). Multiple ace genes encoding acetylcholinesterases of Caenorhabditis elegans have distinct tissue expression. European Journal of Neuroscience 18, 497–512.CrossRefGoogle Scholar
Harel, M., Schalk, I., Ehret-Sabatier, L., Bouet, F., Goeldner, M., Hirth, C., Axelsen, P. H., Silman, I. and Sussman, J. L. ( 1993). Quaternary ligand binding to aromatic residues in the active-site gorge of acetylcholinesterase. Proceedings of the National Academy of Sciences, USA 90, 9031–9035.CrossRefGoogle Scholar
Hussein, A. S., Grigg, M. E. and Selkirk, M. E. ( 1999). Nippostrongylus brasiliensis: characterisation of a somatic amphiphilic acetylcholinesterase with properties distinct from the secreted enzymes. Experimental Parasitology 91, 144–150.CrossRefGoogle Scholar
Hussein, A. S., Harel, M. and Selkirk, M. E. ( 2002). A distinct family of acetylcholinesterases is secreted by Nippostrongylus brasiliensis. Molecular and Biochemical Parasitology 123, 125–134.Google Scholar
Johnson, D. R., Sales, J. and Matthews, J. B. ( 2005). Local cytokine responses in Dictyocaulus viviparus infection. Veterinary Parasitology 128, 309–318.CrossRefGoogle Scholar
Kumar, S., Tamura, K., Jakobsen, I. B. and Nei, M. ( 2001). MEGA2: Molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245.CrossRefGoogle Scholar
Laffaire, J. B., Jaubert, S., Abad, P. and Rosso, M. N. ( 2003). Molecular cloning and life stage expression pattern of a new acetylcholinesterase gene from the plant parasitic nematode, Meloidogyne incognita. Nematology 5, 213–217.CrossRefGoogle Scholar
Lazari, O., Hussein, A. S., Selkirk, M. E., Davidson, A. J., Thompson, F. J. and Matthews, J. B. ( 2003). Cloning and expression of two secretory acetylcholinesterases from the bovine lungworm, Dictyocaulus viviparus. Molecular and Biochemical Parasitology 132, 83–92.CrossRefGoogle Scholar
Lazari, O., Selkirk, M. E., Ploeger, H. W. and Matthews, J. B. ( 2004). A putative neuromuscular acetylcholinesterase gene from Dictyocaulus viviparus. Molecular and Biochemical Parasitology 136, 313–317.CrossRefGoogle Scholar
Lee, D. L. ( 1996). Why do some nematode parasites of the alimentary tract secrete acetylcholinesterase? International Journal for Parasitology 26, 499–508.Google Scholar
Massoulié, J. ( 2002). The origin of the molecular diversity and functional anchoring of cholinesterases. Neurosignals 11, 130–143.CrossRefGoogle Scholar
Massoulié, J., Anselmet, A., Bon, S., Krejci, E., Legay, C., Morel, N. and Simon, S. ( 1998). Acetylcholinesterase: C-terminal domains, molecular forms and functional localization. Journal of Physiology 92, 183–190.CrossRefGoogle Scholar
McKeand, J. B., Knox, D. P., Duncan, J. L. and Kennedy, M. W. ( 1994). The immunogenicity of the acetylcholinesterases of the cattle lungworm, Dictyocaulus viviparus. International Journal for Parasitology 24, 501–510.CrossRefGoogle Scholar
Piotte, C., Arthaud, L., Abad, P. and Rosso, M. N. ( 1999). Molecular cloning of an acetylcholinesterase gene from the plant parasitic nematodes, Meloidogyne incognita and Meloidogyne javanica. Molecular and Biochemical Parasitology 99, 247–256.CrossRefGoogle Scholar
Selkirk, M. E., Lazari, O., Hussein, A. S. and Matthews, J. B. ( 2005). Nematode acetylcholinesterases are encoded by multiple genes and perform non-overlapping functions. Chemico-biological Interactions 157–158, 263–268.CrossRefGoogle Scholar
Sussman, J. L., Harel, M., Frolow, F., Oefner, C., Goldman, A., Toker, L. and Silman, I. ( 1991). Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science 253, 872–879.CrossRefGoogle Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. ( 1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4670–4680.CrossRefGoogle Scholar